Morph-Dependent Expression and Subcellular Localization of Host Serine Carboxypeptidase in Bacteriocytes of the Pea Aphid Associated with Degradation of the Endosymbiotic Bacterium Buchnera

Abstract

Pea aphids form a mutualistic association with the endosymbiotic bacterium Buchnera, which is harbored in specialized host cells called bacteriocytes. The adult aphids display dimorphism In which there are winged and wingless morphs. We previously reported that the Buchnera density in bacteriocytes of the winged morph (alate) decreases around final ecdysis, whereas that in the wingless morph (aptera) does not decrease; the decrease in density in alatae is accompanied by activation of the host lysosomal system and by Buchnera degradation. In the present study, we performed a proteomic analysis to clarify the molecular mechanisms underlying the decrease in Buchnera density. By comparing the protein expression profiles of bacteriocytes in alatae and apterae Just after final ecdysis, we identified three and one protein spots that were preferentially expressed in alatae and apterae, respectively. Among the three alate-preferential spots, two were an identical aphid protein, carboxypeptidase vitellogenic-like (CPVL), whereas the other was a mixture of four proteins: gamma-glutamyl hydrolase, acyl-CoA dehydrogenase, aphid short chain acyl-CoA dehydrogenase, and Buchnera S-adenosylmethionine synthetase. The aptera-preferential spot was Buchnera outer membrane protein A. Immunoblot and immunohistochemical analyses using aphid bacteriocytes Just after final ecdysis revealed that expression of aphid CPVL was preferentially upregulated in alatae and was localized around Buchnera cells in the bacterlocytes, suggesting the involvement of CPVL in Buchnera degradation in alatae.

Bacteriocyte dynamics during development of a holometabolous insect, the carpenter ant Camponotus floridanus

“…In these animals about two weeks after ecdysis the bacterial load decreases strongly. A cytochemical analysis revealed the presence of lysosome-like acidic organelles in the bacteriocytes and an upregulation of lysosome-related genes around final ecdysis [22,23]. Electron microscopic analysis of the aphid tissue in these stages revealed a different morphology of the symbiosomes, suggesting degradation of the endosymbionts by the lysosomal system.…”

“…The number of Buchnera in A. pisum may be actively downregulated by the host about two weeks after final ecdysis. The decrease in symbiont number was shown to be correlated with an activation of the lysosomal system of the bacteriocytes [22,23]. …”

Host Plant Determines the Population Size of an Obligate Symbiont (Buchnera aphidicola) in Aphids

“…The data indicate that plant secondary metabolites might influence endosymbiont dynamics in herbivorous insects. The host plant might influence Buchnera dynamics directly or indirectly through the aphid host, for example, by effects on the expression of aphid carboxypeptidase vitellogenic-like protein or by affecting bacteriocyte development and lysozyme production (48,49). The second hypothesis is that the host may manipulate its endosymbiont titer to compensate for specific deficiencies in the nutrient profile of its host plant (8,50,51).…”

Comparative gut transcriptome analysis reveals differences between virulent and avirulent Russian wheat aphids, Diuraphis noxia

“…Nishikori et al (2009) demonstrated the involvement of an A. pisum carboxypeptidase in Buchnera degradation, and for this reason, we hypothesize that the observed over-expression of carboxypeptidases in RWA1 may lead to Buchnera degradation and a resulting deficiency of essential amino acids vital for RWA1 survival.…”